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. 2020 Apr 8;287(1924):20192736.
doi: 10.1098/rspb.2019.2736. Epub 2020 Apr 8.

Global shifts in mammalian population trends reveal key predictors of virus spillover risk

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Global shifts in mammalian population trends reveal key predictors of virus spillover risk

Christine K Johnson et al. Proc Biol Sci..

Abstract

Emerging infectious diseases in humans are frequently caused by pathogens originating from animal hosts, and zoonotic disease outbreaks present a major challenge to global health. To investigate drivers of virus spillover, we evaluated the number of viruses mammalian species have shared with humans. We discovered that the number of zoonotic viruses detected in mammalian species scales positively with global species abundance, suggesting that virus transmission risk has been highest from animal species that have increased in abundance and even expanded their range by adapting to human-dominated landscapes. Domesticated species, primates and bats were identified as having more zoonotic viruses than other species. Among threatened wildlife species, those with population reductions owing to exploitation and loss of habitat shared more viruses with humans. Exploitation of wildlife through hunting and trade facilitates close contact between wildlife and humans, and our findings provide further evidence that exploitation, as well as anthropogenic activities that have caused losses in wildlife habitat quality, have increased opportunities for animal-human interactions and facilitated zoonotic disease transmission. Our study provides new evidence for assessing spillover risk from mammalian species and highlights convergent processes whereby the causes of wildlife population declines have facilitated the transmission of animal viruses to humans.

Keywords: exploitation; habitat loss; spillover; threatened species; virus; zoonotic disease.

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Conflict of interest statement

The authors have no competing interests.

Figures

Figure 1.
Figure 1.
Richness of zoonotic viruses found in mammalian hosts, by taxonomic order for wildlife and by species for domesticated animals and humans. (a) Zoonotic virus richness corresponding to species richness among wild mammalian orders. Area of the circles represents the proportion of zoonotic viruses found in species in each order out of the total number of zoonotic viruses among all mammalian species. Orders with less than 5% of zoonotic viruses and less than 2% of mammalian species include Didelphimorphia, Pilosa, Proboscidea, Diprotodontia, Perissodactyla, Cingulata and Dasyuromorphia are not labelled. (b) Zoonotic virus richness corresponding to estimated global abundance (in millions) for humans [15] and domesticated species [16]. Species are coloured according to the order in which they belong in (a). Area of the circles reflects the estimated population size for that species relative to the other species shown. (Online version in colour.)
Figure 2.
Figure 2.
Number of mammalian viruses shared with humans for each taxonomic order by IUCN threatened species criteria. The number of zoonotic viruses reported in threatened wildlife species, shown by relative circle area for each taxonomic order according to the scale shown. Scale of circle areas range from one virus (as exemplified by criteria D1 for Artiodactyla) to 16 viruses (as exemplified by criteria A1–A4(c) for primates). Numbers of viruses are not adjusted for factors found to be related to species virus counts in multivariable regression modelling. Species in each order were categorized by the IUCN Red List criteria as adapted for this study. Refer to the IUCN Red List categories and criteria for a detailed explanation of the criteria used by the IUCN to evaluate species trends and place species into threatened categories [14]. (Online version in colour.)
Figure 3.
Figure 3.
Bipartite network showing wild and domesticated mammalian species and their zoonotic virus associations. Host species harbouring the same zoonotic virus are linked by shared zoonotic viruses (grey nodes). Mammalian species nodes are coloured by domestication status and taxonomic order for non-domesticated terrestrial wildlife as shown. Species node size is relative to the zoonotic virus richness calculated in that species. Humans, who are host to all viruses, are not shown. (Online version in colour.)

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